Arabidopsis is an important model organism in plant biology and genetics, and a large number of a chromatin conformation and epigenomic datasets have been generated to study the biology in Arabidopsis. To make it easier to access the accumulated epigenomic data, a user-friendly and reproducible epigenomic database, AraENCODE was developed. It contains various datasets and resources, including chromatin conformation, epigenomic, and transcriptome data, allowing researchers to investigate the regulation of epigenetic and chromatin interactions in Arabidopsis.

SnRK1, an evolutionarily conserved heterotrimeric kinase complex that acts as a key metabolic sensor in maintaining energy homeostasis in plants, is an important upstream activator of autophagy that serves as a cellular degradation mechanism for the healthy growth of plants. However, whether and how the autophagy pathway is involved in regulating SnRK1 activity remains unknown. In this study, we identified a clade of plant-specific and mitochondria-localized FCS-like zinc finger (FLZ) proteins as currently unknown ATG8-interacting partners that actively inhibit SnRK1 signaling by repressing the T-loop phosphorylation of the catalytic α subunits of SnRK1, thereby negatively modulating autophagy and plant tolerance to energy deprivation caused by long-term carbon starvation. Interestingly, these AtFLZs are transcriptionally repressed by low-energy stress, and AtFLZ proteins undergo a selective autophagy-dependent pathway to be delivered to the vacuole for degradation, thereby constituting a positive feedback regulation to relieve their repression of SnRK1 signaling. Bioinformatic analyses show that the ATG8-FLZ-SnRK1 regulatory axis first appears in gymnosperms and seems to be highly conserved during the evolution of seed plants. Consistent with this, depletion of ATG8-interacting ZmFLZ14 confers enhanced tolerance, whereas overexpression of ZmFLZ14 leads to reduced tolerance to energy deprivation in maize. Collectively, our study reveals a previously unknown mechanism by which autophagy contributes to the positive feedback regulation of SnRK1 signaling, thereby enabling plants to better adapt to stressful environments.

Vascular cambium produces the phloem and xylem, vascular tissues that transport resources and provide mechanical support, making it an ideal target for crop improvement. However, much remains unknown about how vascular cambium proliferates. In this study, through pharmaceutical and genetic manipulation of reactive oxygen species (ROS) maxima, we demonstrate a direct link between levels of ROS and activity of LATERAL ORGAN BOUNDARIES DOMAIN 11 (LBD11) in maintaining vascular cambium activity. LBD11 activates the transcription of several key ROS metabolic genes, including PEROXIDASE 71 and RESPIRATORY BURST OXIDASE HOMOLOGS D and F, to generate local ROS maxima in cambium, which in turn enhance the proliferation of cambial cells. In a negative feedback mechanism, higher ROS levels then repress LBD11 expression and maintain the balance of cambial cell proliferation. Our findings thus reveal the role of a novel LBD11/ROS-dependent feedback regulatory system in maintaining vascular cambium-specific redox homeostasis and radial growth in plants.

Although the plant kingdom provides an enormous diversity of metabolites with potentially beneficial applications for humankind, a large fraction of these metabolites and their biosynthetic pathways remain unknown. Resolving metabolite structures and their biosynthetic pathways is key to gaining biological understanding and to allow metabolic engineering. In order to retrieve novel biosynthetic genes involved in specialized metabolism, we developed a novel untargeted method designated as qualitative trait GWAS (QT-GWAS) that subjects qualitative metabolic traits to a genome-wide association study, while the conventional metabolite GWAS (mGWAS) mainly considers the quantitative variation of metabolites. As a proof of the validity of QT-GWAS, 23 and 15 of the retrieved associations identified in Arabidopsis thaliana by QT-GWAS and mGWAS, respectively, were supported by previous research. Furthermore, seven gene-metabolite associations retrieved by QT-GWAS were confirmed in this study through reverse genetics combined with metabolomics and/or in vitro enzyme assays. As such, we established that CYTOCHROME P450 706A5 (CYP706A5) is involved in the biosynthesis of chroman derivatives, UDP-GLYCOSYLTRANSFERASE 76C3 (UGT76C3) is able to hexosylate guanine in vitro and in planta, and SULFOTRANSFERASE 202B1 (SULT202B1) catalyzes the sulfation of neolignans in vitro. Collectively, our study demonstrates that the untargeted QT-GWAS method can retrieve valid gene-metabolite associations at the level of enzyme-encoding genes, even new associations that cannot be found by the conventional mGWAS, providing a new approach for dissecting qualitative metabolic traits.

Pod coloration is a domestication-related trait in soybean, with modern cultivars typically displaying brown or tan pods, while their wild relative, Glycine soja, possesses black pods. However, the factors regulating this color variation remain unknown. In this study, we cloned and characterized L1, the classical locus responsible for black pods in soybean. By using map-based cloning and genetic analyses, we identified the causal gene of L1 and revealed that it encodes a hydroxymethylglutaryl-coenzyme A (CoA) lyase-like (HMGL-like) domain protein. Biochemical assays showed that L1 functions as a eucomic acid synthase and facilitates the synthesis of eucomic acid and piscidic acid, both of which contribute to coloration of pods and seed coats in soybean. Interestingly, we found that L1 plants are more prone to pod shattering under light exposure than l1 null mutants because dark pigmentation increases photothermal efficiency. Hence, pleiotropic effects of L1 on pod color and shattering, as well as seed pigmentation, likely contributed to the preference for l1 alleles during soybean domestication and improvement. Collectively, our study provides new insights into the mechanism of pod coloration and identifies a new target for future de novo domestication of legume crops.

The open reading regions of ZmPHT1s (inorganic phosphate [Pi] transporters) in maize possess target sites of microRNA399 (miR399). However, the relationship between miR399 and ZmPHT1s and its functional importance in response to Pi deficiency remain to be explored. We show here that ZmPHT1;1, ZmPHT1;3, and ZmPHT1;13 are the targets of ZmmiRNA399. We found that a long non-coding RNA, PILNCR2 (Pi-deficiency-induced lncRNA 2), is transcribed from the opposing DNA strand of ZmPHT1;1 and predominantly localized in the cytoplasm. A ribonuclease protection assay and an RNA-RNA binding assay showed that PILNCR2 and ZmPHT1s could form the RNA/RNA duplexes in vivo and in vitro. A co-expression assay in N. benthamiana revealed that the PILNCR2/ZmPHT1 RNA/RNA duplexes interfere with miR399-guided cleavage of ZmPHT1 mRNAs. Overexpression of PILNCR2 increased low-Pi tolerance in maize, whereas its knockout and knockdown decreased low-Pi tolerance in maize. Consistently, ZmPHT1;3 and ZmPHT1;13 mRNA abundance was increased in transgenic plants overexpressing PILNCR2 but reduced in its knock-out mutants, suggesting that PILNCR2 positively regulates the mRNA abundance of ZmPHT1;3 and ZmPHT1;13 in maize. Collectively, these results indicate that PILNCR2 plays an important role in maize Pi homeostasis by interfering with miRNA399-guided cleavage of ZmPHT1 mRNAs.

Growth- and health-promoting bacteria can boost crop productivity in a sustainable way. Pseudomonas simiae WCS417 is such a bacterium that efficiently colonizes roots, modifies the architecture of the root system to increase its size, and induces systemic resistance to make plants more resistant to pests and pathogens. Our previous work suggested that WCS417-induced phenotypes are controlled by root cell-type-specific mechanisms. However, it remains unclear how WCS417 affects these mechanisms. In this study, we transcriptionally profiled five Arabidopsis thaliana root cell types following WCS417 colonization. We found that the cortex and endodermis have the most differentially expressed genes, even though they are not in direct contact with this epiphytic bacterium. Many of these genes are associated with reduced cell wall biogenesis, and mutant analysis suggests that this downregulation facilitates WCS417-driven root architectural changes. Furthermore, we observed elevated expression of suberin biosynthesis genes and increased deposition of suberin in the endodermis of WCS417-colonized roots. Using an endodermal barrier mutant, we showed the importance of endodermal barrier integrity for optimal plant-beneficial bacterium association. Comparison of the transcriptome profiles in the two epidermal cell types that are in direct contact with WCS417-trichoblasts that form root hairs and atrichoblasts that do not-implies a difference in potential for defense gene activation. While both cell types respond to WCS417, trichoblasts displayed both higher basal and WCS417-dependent activation of defense-related genes compared with atrichoblasts. This suggests that root hairs may activate root immunity, a hypothesis that is supported by differential immune responses in root hair mutants. Taken together, these results highlight the strength of cell-type-specific transcriptional profiling to uncover "masked" biological mechanisms underlying beneficial plant-microbe associations.

The disciplines of evolutionary biology and plant and animal breeding have been intertwined throughout their development, with responses to artificial selection yielding insights into the action of natural selection and evolutionary biology providing statistical and conceptual guidance for modern breeding. Here we offer an evolutionary perspective on a grand challenge of the 21st century: feeding humanity in the face of climate change. We first highlight promising strategies currently under way to adapt crops to current and future climate change. These include methods to match crop varieties with current and predicted environments and to optimize breeding goals, management practices, and crop microbiomes to enhance yield and sustainable production. We also describe the promise of crop wild relatives and recent technological innovations such as speed breeding, genomic selection, and genome editing for improving environmental resilience of existing crop varieties or for developing new crops. Next, we discuss how methods and theory from evolutionary biology can enhance these existing strategies and suggest novel approaches. We focus initially on methods for reconstructing the evolutionary history of crops and their pests and symbionts, because such historical information provides an overall framework for crop-improvement efforts. We then describe how evolutionary approaches can be used to detect and mitigate the accumulation of deleterious mutations in crop genomes, identify alleles and mutations that underlie adaptation (and maladaptation) to agricultural environments, mitigate evolutionary trade-offs, and improve critical proteins. Continuing feedback between the evolution and crop biology communities will ensure optimal design of strategies for adapting crops to climate change.

Global climate change exacerbates the effects of environmental stressors, such as drought, flooding, extreme temperatures, salinity, and alkalinity, on crop growth and grain yield, threatening the sustainability of the food supply. Maize (Zea mays) is one of the most widely cultivated crops and the most abundant grain crop in production worldwide. However, the stability of maize yield is highly dependent on environmental conditions. Recently, great progress has been made in understanding the molecular mechanisms underlying maize responses to environmental stresses and in developing stress-resilient varieties due to advances in high-throughput sequencing technologies, multi-omics analysis platforms, and automated phenotyping facilities. In this review, we summarize recent advances in dissecting the genetic factors and networks that contribute to maize abiotic stress tolerance through diverse strategies. We also discuss future challenges and opportunities for the development of climate-resilient maize varieties.